Ann Thorac Surg 2004;78:173-180
© 2004 The Society of Thoracic Surgeons
Original article: cardiovascular
Establishing right ventricle-pulmonary artery continuity by autologous tissue: an alternative approach for prosthetic conduit repair
Yukihisa Isomatsu, MDa*,
Toshiharu Shin'oka, MDa,
Mitsuru Aoki, MDa,
Masatsugu Terada, MDa,
Takamasa Takeuchi, MDa,
Shuichi Hoshino, MDa,
Yoshinori Takanashi, MDa,
Yasuharu Imai, MDa,
Hiromi Kurosawa, MDa
a Department of Cardiovascular Surgery, The Heart Institute of Japan, Tokyo Women's Medical University, Tokyo, Japan
Accepted for publication November 25, 2003.
* Address reprint requests to Dr Isomatsu, Department of Surgery, Yokohama City University School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama 236-0004, Japan
e-mail: isomatsu{at}med.yokohama-cu.ac.jp
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Abstract
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BACKGROUND: In conventional conduit operations, longevity has been essentially limited by the inevitable need for conduit replacement. This study was undertaken to compare long-term results of the use of equine pericardial conduits, autologous pericardial conduits, and direct anastomosis repair.
METHODS: Between 1982 and 2001, 366 patients underwent primary establishment of right ventricle-pulmonary artery continuity at our institution. The mean age at the time of operation was 6.2 years (range, 4 days to 28 years) and mean weight was 17.2 kg (range, 1.6 to 61 kg). Three different repair techniques were used for connection: hand-made valved equine pericardial conduits (n = 179), autologous pericardial conduits (n = 71), and direct anastomosis without a conduit (n = 116). Mean follow-up period for early survivors was 8.6 years in the equine group, 6.1 years in the direct anastomosis group, and 5.1 years in the autologous pericardium group.
RESULTS: Direct anastomosis repair (p = 0.0002) was associated with significantly better freedom from late events (conduit replacement or late death) than equine pericardial conduits. The hazard ratio was less with the autologous pericardium conduit than with the equine pericardium, but the difference was not statistically significant (p = 0.2122). Younger age at operation, and postoperative pressure ratio from right to left ventricle were also predictors of conduit longevity.
CONCLUSIONS: To decrease the probability of late events, direct anastomosis is an encouraging technique compared with traditional equine pericardium extracardiac conduit repair. An autologous pericardial conduit, because of its benefits, would be an alternative when direct anastomosis is not suitable.
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Introduction
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There essentially has been no change in the surgical approach to correct discontinuities between the right ventricle (RV) and the pulmonary artery (PA) since Rastelli and colleagues [1] used a nonvalved pericardial conduit and Ross and Somerville [2] used a homograft. The interposition of a valved conduit has been commonly performed to establish RV-PA continuity. However, several studies have demonstrated limitations in conduit longevity with conduit replacement being inevitable [3–7]. Techniques of repair that avoid the use of conduits or that do not require future repairs should be investigated. In this study, we compare the long-term results of equine pericardial conduits with those achieved using direct anastomosis or autologous pericardial conduit repair.
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Patients and methods
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Between January 1982 and December 2001, 366 patients underwent the primary establishment of an RV-PA continuity at the Heart Institute of Japan (Tokyo Women's Medical University, Japan). Of these patients, 184 were males (50.3%) and 182 were females (49.7%) with a mean age ± standard deviation (SD) of 6.2 ± 5.3 years (range, 4 days–28 years; median, 4.9 years) and mean weight ± SD of 17.2 ± 11.2 kg (range, 1.6 to 61 kg; median, 15.0 kg) at the time of operation. Three different repair procedures were used to connect the RV and the PA (Fig 1).
Hand-made valved equine pericardial conduits (n = 179), direct anastomosis without a conduit (n = 116), and fresh autologous pericardial conduits (n = 71) were used. The median ages at operation within each treatment group were 5.6 years in the equine pericardium group, 4.1 years for direct anastomosis, and 4.8 years in the autologous pericardial conduit recipients.
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Fig 1. Distribution of conduit types used in our institution during four-year intervals between 1982 and 2001. Solid areas = direct anastomosis; grey areas = autologous pericardium; open areas = equine pericardium.
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The diagnoses were tetralogy of Fallot with pulmonary atresia (TOF-PA) in 91 patients, major aortopulmonary collateral arteries and pulmonary atresia with ventricular septal defect (MAPCA) in 74 patients, transposition of the great arteries, ventricular septal defect and pulmonary stenosis (TGA-VSD-PS) in 67 patients, atrioventricular discordance (AVD) in 63 patients; truncus arteriosus in 39 patients, and double-outlet right ventricle (DORV) in 32 patients (Table 1).
The first three diagnoses were the most common, comprising almost two-thirds of the patients. Among the 74 MAPCA patients, unifocalization repair was performed 122 times [8], as a preparatory operation. Since 1990, anatomic corrections (combination of atrial switch and conduit repair from the anatomical RV to PA) were performed in the 63 AVD patients [9]. Twenty-seven conventional extracardiac conduit operations in an earlier series were excluded from this analysis because the conduit was placed between the apex of the anatomical left ventricle and the PA. Before their corrections, 141 patients (38.5%) had undergone one palliative operation, and 116 patients (31.7%) had two or more palliative surgeries consisting primarily of a systemic to pulmonary shunt.
Equine pericardial conduits
Since January 1982, handmade tricuspid conduits were placed in 179 patients. This valved conduit, made of equine pericardium preserved in glutaraldehyde (Xenomedica, Baxter, IL), was created over a Hegar dilator of appropriate diameter ranging from 14 to 26 mm. The diameter of the conduit was chosen according to the patient's body weight (BW): 14 mm for BW less than or equal to 4 kg, 18 mm for 4 less than BW less than or equal to 7 kg, 22 mm for 7 less than BW less than or equal to 15 kg, and 26 mm for BW more than 15 kg. The valvular portion had three semilunar cusps and a subvalvular skirt that was reinforced by thin Dacron (du Pont de Nemours and Co.) velour. This conduit was designated to have the suture line of the tubular portion directed posteriorly.
Direct anastomosis or autologous pericardial conduits
Our current surgical policy is to use direct anastomosis, when possible, between the PA and the RV by bringing down the distal end of the PA to the ventriculotomy and covering the anterior aspect of the outflow tract with an autologous pericardial monocuspid patch (Figs 2 and 3).
When a direct anastomosis is impossible, an autologous pericardial conduit bearing one cusp is placed between the PA and the ventricle (Fig 2).
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Fig 2. Direct anastomosis (A, B) and interposition of an autologous pericardial conduit (C). (A) The distal pulmonary arteries were extensively mobilized as far as both hilar regions to expose the origin of the upper lobar branches. The pulmonary artery was brought on the left side of the aorta. An incision in the anterior pulmonary artery was made into the left pulmonary artery in a reversed J shape. A direct anastomosis was performed at the cranial margin of the ventriculotomy incision using several pledgeted mattress sutures. (B) The outflow tract was enlarged by a monocuspid autologous pericardial patch reinforced with Dacron material. (C) After patch angioplasty was completed, if necessary, the autologous pericardial patch was made tubular by approximating its lateral edges, creating an anterior wall long enough to cover the ventricular incision. A single cusp was sutured on its inner anterior wall, and the subvalvular portion was reinforced with Dacron.
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Fig 3. Detailed drawing of the construction of the monocusped autologous pericardial patch. (A) Autologous pericardium is trimmed into semicircular shape (H = 1/2R). (B) Similar figure of semicircle made at (A), at 2/3 the size (R' = 2/3R, H' = 2/3H). (C) The cusp width is R'. Cusp height is H', where H' is approximately 3/4H'. Thus, this height H' corresponds to almost one-half of H. Two stay stitches are placed at both lateral ends and a third stitch is placed at the bottom of the cusp. (D) The smooth surface (the serous layer) of the cusp should be oriented to the sinus. The smooth surface of the remaining rectangle pericardium should be the inner surface of the monocuspid patch.
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Of 261 consecutive cases since January 1990, when all three methods were available (Table 1), direct anastomoses were performed in 112 patients (42.9%) and an autologous pericardial conduit was used in 71 patients (27.2%). When stratified according to diagnosis, the highest rate of direct anastomosis was performed for TOF-PA and the highest rate of autologous pericardial conduit was performed for MAPCA. In all five eras and the last three eras, the highest rate of equine pericardial conduit was performed for truncus.
Follow-up
Postoperative right-to-left ventricular pressure ratio (RVP-LVP) was measured in the operating room before chest closure in 302 patients. Follow-up data of a patient who underwent a total correction before December 1998 was considered complete if the patient visited our outpatient unit after January 2000. Follow up of a patient having surgery after January 1999 was considered complete if the patient's status was determined after January 2001. A total of 91.8% of survivors completed follow up.
Statistical analysis
Early mortality was defined as death within 30 days of total correction, or death during the same hospitalization for total correction. Preoperative variables for early mortality were evaluated by means of univariate and multivariate logistic regression analysis. Transformations were performed because the natural logarithm of age at operation was a better predictor than age itself. In the analysis of late outcomes, the two endpoints evaluated were patient death and conduit failure requiring replacement. Indications for conduit replacement were either a pressure gradient greater than or equal to 50 mm Hg between the right ventricle and the PA, or infection of the conduit. No patient underwent conduit replacement with the indication of regurgitation alone. Patients who did not die or did not have conduit replacement were considered to be censored at the time of last follow up. Time-related events were examined by Kaplan-Meier methods. Preoperative factors and postoperative RVP-LVP were assessed by multivariate analysis using a Cox proportional hazards regression model. For analyses of freedom from late events, time of total correction was taken as time zero. The RV function for the three different methods was analyzed by two-way repeated-measures analysis of variance (ANOVA) in terms of RV end-diastolic volume (RVEDV) and RV ejection fraction (RVEF). The RVEDV was calculated as a percentage of expected normal value according to the method described by Nakazawa and colleagues [10]. Preoperative and postoperative catheterization data of the same patient (mean interval; 1.35 ± 0.97 years) were available for 185 patients. A value of p less than 0.05 was considered statistically significant. Data computations were performed using the StatView 5.0 (SAS Institute Inc., Cary, NC) statistical program.
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Results
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Early mortality
Among the 366 patients, there were 38 early deaths (9.0%, 95% confidence interval (CI) 6.8% to 12.2%). There were 25 early deaths in the equine pericardium group (14.0%, 95% CI 8.9% to 19.0%), 8 in the direct anastomosis group (6.9%, 95% CI 2.3% to 11.5%), and 5 in the autologous pericardium group (7.0%, 95% CI 1.1% to 12.9%). As shown in Table 2,
multivariate analysis demonstrated a significant association between early mortality and the following variables: truncus, younger age at the time of total correction, and earlier period of surgery. Neither direct anastomosis nor autologous pericardium had a significant association with early mortality compared with equine pericardium.
Late events
Mean follow-up period ± SD of early survivors was 8.6 ± 4.3 years (range, 0.1 to 16.9 years; median, 9.4 years) in the equine group, 6.1 ± 3.3 years (range, 0.41 to 16.7 years; median, 6.6 years) in the group having undergone direct anastomosis, and 5.1 ± 3.2 years (range, 0.12 to 10.3 years; 5.4 years) in the autologous pericardium group. Ninety-seven late events (78 conduit replacements [CR] and 19 late deaths [LD]) occurred in the equine group, 10 late events (4 CR and 6 LD) in the direct anastomosis group, and 8 late events (8 LD) in the autologous pericardium group. Of 82 CR, three were due to conduit infection. Details of late events are shown in Table 3.
Pulmonary vascular resistance (PVR) was significantly higher in LD than that in the early survivors in the truncus group in comparison with early survivors and LD in any of the other diagnoses. The truncus patients also had the highest rate of late events. Plots of Kaplan-Meier estimates of freedom from late events stratified by method (Fig 4)
were as follows: 91.6% at 5 years and 88.6% at 10 years in direct anastomosis; 88.5% at 5 years and 85.4% at 10 years in autologous pericardium; and 83.7% at 5 years, 52.8% at 10 years, and 15.7% at 15 years in equine pericardium. Direct anastomosis repairs had significantly better freedom from late events than repairs using equine pericardium. There was no significant difference in freedom from late events between autologous pericardium and equine pericardium repairs. In other categories, risk factors for late events included younger age at the time of total correction, an increased postoperative RVP-LVP, and some cardiac diagnoses (Table 4).
Date of surgery did not have a significant association with the occurrence of late events.
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Table 3. Relation Between Late Death, Late Events, and Pulmonary Vascular Resistance Stratified According to Diagnosis
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Fig 4. Kaplan-Meier freedom from late events (conduit replacement or late death) stratified by method. Number of patients at risk in follow-up period stratified by method is shown in parentheses at selected time points. Early mortality is excluded in this analysis.
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Overall mortality in grouping according to method (Fig 5)
were as follows: 87.4% at both 5 years and at 10 years in direct anastomosis; 81.0% at 5 years and 77.8% at 10 years in autologous pericardium; and 78.9% at 5 years, 74.6% at 10 years, and 73.0% at 15 years in equine pericardium.
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Fig 5. Kaplan-Meier patient survival rate stratified by method. Number of patients at risk in follow-up period stratified by method is shown in parentheses at selected time points. There was no significant difference among three groups by log-rank test (p = 0.111). Early mortality is also included in this analysis.
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RV function
There was no statistically significant change in RVEDV between preoperative and postoperative values for RVEDV for any of the three methods (Fig 6A,
p = 0.605). Nor were there statistically significant differences in RVEDV among the three different methods at either the preoperative and postoperative time point (Fig 6A, p = 0.972). With regard to RVEF, there was no significant difference in either the preoperative or postoperative values among the three methods (Fig 6B, p = 0.646), although there was a significant change in RVEF between preoperative and postoperative values in the method of equine pericardium (Fig 6B, p = 0.0013).
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Fig 6. Preoperative and postoperative right ventricular end-diastolic volume (RVEDV, A) and right ventricular ejection fraction (RVEF, B) grouped by methods. (A) There was no significant change in RVEDV between preoperative and postoperative values in each method (p = 0.605). There was no significant difference in preoperative RVEDV among the three different methods and no significant difference in postoperative RVEDV among the three methods (p = 0.972). (B) There was no significant difference in either the preoperative or postoperative values among the three methods (B, p = 0.646), although there was a significant change in RVEF between preoperative and postoperative values in the method of equine pericardium (B, p = 0.0013). Open bars = preoperative; grey bars = postoperative.
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Comment
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Direct anastomosis repair (p = 0.0002) had a significantly smaller hazard ratio for late events than equine pericardium conduit repair. The valved equine conduits did not possess the longevity we had expected (Fig 4), although they were used from 1982 to 1993. Causes of conduit failure in the valved equine conduits were hardening of the valve with calcification and luminal stenosis due to neointimal overgrowth [11]. This smaller hazard ratio of direct anastomosis supports our assumption that these tissue reactions are less likely to occur in direct anastomosis. These factors suggest that we should choose direct anastomosis when applicable, considering that preoperative RV function and postoperative RV function had no significant difference among the three different methods.
Although the hazard ratio for autologous pericardial conduit repair did not differ significantly from that of equine pericardium conduit repair by multivariate analysis (Table 4), autologous pericardial conduit repair has several advantages. First, no antigenicity was observed with the autologous pericardial conduit because it consists of the patient's own tissue. Second, reconstruction using an autologous pericardial conduit is less expensive than with the equine pericardial conduit. Third, autologous pericardial conduit repair has good long-term results [12, 13]. Thus, we believe that autologous pericardial conduit repair would be an alternative when direct anastomosis is not applicable.
Whether direct anastomosis is possible is another concern. We usually perform repair with an autologous pericardial conduit in the following two situations: (1) when the distal pulmonary artery is severely hypoplastic or nonconfluent with a long distance between the pulmonary artery and the ventriculotomy, as this typically requires extensive patch angioplasty, and (2) when the left coronary artery has a high take-off origin, so as to avoid compression of the left coronary artery by the new pulmonary trunk after direct anastomosis. In our clinical experience, there was a greater usage of autologous pericardial conduit than direct anastomosis for MAPCA because with MAPCA there was often a long distance from the RV to the PA (Table 1). For truncus, which has been associated with a higher PVR and a higher incidence of late events (Table 3), our current strategy is to establish RV-PA continuity by equine pericardial conduit particularly early in infancy at the first operation, and thereafter to reestablish RV-PA continuity by autologous tissue at the second operation in the late period.
The concept of anastomosing a distal pulmonary arterial stump directly to the right ventricular incision was similar to the REV procedure introduced by Lecompte and colleagues [14, 15]. We extended this concept of autologous tissue reconstruction to other diseases with pulmonary outflow tract obstruction. We modified the procedure so that the newly reconstructed pulmonary outflow tract locates around the left side of the aorta without an anterior translocation of the pulmonary bifurcation. The aim of this modification is to avoid anterior bulging of the ascending aorta, which may later cause pulmonary stenosis. In reports of Lecompte [15], as well as Vouhé and colleagues [16], the actuarial freedom from reoperation was 85.4% at 5 years and 85% at 7 years, respectively, in patients with complete transposition, ventricular septal defect, and pulmonary outflow tract obstruction. These values are similar to our result of 88.6% at 10 years after a direct anastomosis (although our result of 88.6% also included late deaths) for transposition and other complex forms of pulmonary outflow tract obstruction.
Age has been reported to be an important predictor of conduit longevity or valve survival in other studies [4, 6, 7]. In conventional conduit operations, since the child grows and the conduit remains unchanged in size, there is an essential limitation to longevity with the inevitable need for conduit replacement. Also in this study, age at operation itself had a significant association with late events. Thus, at present, we should be careful to characterize the direct anastomosis as having "a clear potential for growth," which Vouhé and colleagues cited in their paper [16]. Frequency of conduit replacement, however, may be reduced with the introduction of direct anastomosis after a longer follow-up period than that of the current study.
Postoperative RVP-LVP was also identified to be an independent risk factor for late events in this study, with an estimated hazard ratio of 1.128 per 0.1 U of RVP-LVP increase (Table 4). In order to obtain a lower postoperative RVP-LVP, attention must be given to the following issues: (1) proper performance of the systemic-pulmonary shunt; (2) relief of any stenosis at the connecting site of the patent ductus or systemic-pulmonary shunt, using pulmonary artery angioplasty; and (3) extensive dissection of the pulmonary artery as distally as possible, especially when direct anastomosis is adopted. Kirklin and colleagues [17] emphasized the usefulness of measuring postrepair RVP-LVP after tetralogy of Fallot and pulmonary stenosis. We believe that postoperative RVP-LVP is useful and provides significant information after surgical repair in patients with pulmonary outflow tract obstruction.
In this study, late deaths as well as conduit replacements were included as late events. Although late deaths were regarded as censored at the time of death in a study with the largest number of patients [18], valve-related late deaths, at least, should be included as endpoints [19]. Moreover, it is often unclear whether or not a late death is valve related. Therefore, all late deaths should be treated as one endpoint, otherwise the incidence of conduit failure may be underestimated.
The validity of this study of a clinical experience is limited by its retrospective nature. For example, the three different methods described for establishing RV-PA continuity were not allocated randomly, thus the mean follow-up period differed among each group. The distribution of the three methods varied when stratified according to diagnosis, and thus a low usage of direct anastomosis for truncus and MAPCA may create bias in terms of late events. Multivariate analyses, however, were performed to adjust the influence of these factors. We believe that this experience may provide surgeons with some information regarding long-term morbidity of patients who underwent conduit repair.
In conclusion, to decrease the probability of late events such as conduit replacement and late death, direct anastomosis is an encouraging technique for establishing RV-PA continuity compared with extracardiac equine pericardial conduit repair. An autologous pericardial conduit, when direct anastomosis is not suitable, may be an alternative in some situations. This study suggests potential advantages of autologous tissue reconstruction. However, a longer follow-up period is necessary to clarify its superiority with regard to conduit longevity and to examine possibilities of growth with this approach.
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Acknowledgments
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We thank Dr Shimada Katsunori, Department of Biostatistics, STATZ Corp, for his contribution to the statistical analysis.
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References
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Abstract
Introduction
